2 Main Text
JKB, 29 June 2017 - Before we proceed further, let’s bullet point, our main findings as well as the prevailing views from the field. i.e. We need to very clearly lay out for a highly educated general audience what the expectation was for how corals would respond to heat stress and how what we found differs from the expectation. The expectation part needs to be greatly strengthened in the current draft i.e. we need to set up ‘the mystery’
Here’s what I see as the main discoveries:
Despite unprecedented heat stress, we show that some corals exhibited resilience and survived. Survival through such an extreme heat event provides an exceptional opportunity to understand how some corals can withstand intense heat stress, and how corals in general might survive long-term warming. Remarkably, we find that some coral colonies were able to survive this prolonged heat stress by regaining their symbionts while temperatures were still elevated.
After two months of heat stress, fully-bleached corals retained approximately the same Symbiodinium community as they had before the bleaching event. This suggests that a wholesale breakdown of symbiosis occurred in bleached corals during this event, indicating a lack of preferential symbiont expulsion or exodus.
Symbionts present in even very low abundances can play a critical role in coral survival and recovery. Some coral colonies recovered symbiosis with Symbiodinium types that were present in only a negligible amount before the bleaching event.
Local protection is critical for coral symbiosis and survival. Corals living at different levels of local human disturbance had distinct symbiont communities that corresponded tightly to survivorship. Our results suggest that some Kiritimati coral species may have the capacity to experience evolutionary rescue, defined as adaptation at a rate that allows an endangered population to survive the rate of environmental change (Orr & Unkless 2014, Carlson 2014). Our results suggest that the capacity for evolutionary rescue is tangibly related to local reef protection.
Danielle to write out here a section of bullet points on - ‘What is expected to happen to corals during heat stress?’ (this can include bullets on prevailing viewpoints, bullets on observations from previous heat stress events or from this heat stress event in other locations (e.g. Hughes - GBR), along with the relevant citations).
For example: 1. The prevailing viewpoint is that corals subject to elevated temperatures expel their symbionts and bleach…. (general statement here, including over what time period, and that they can recover their symbionts once the heat stress subsides). General points about the intensity / length /DHW that corals are thought to bleach at, are thought to survive through, or conversely thought to die from e.g. ‘Corals do not typically survive more than X months of Y-Z degrees of elevated temperatures’ - do we know what the most intense heat stress is that corals have previously been documented to survive through?
Prevailing viewpiont is that when coral colonies expel their symbionts, they preferentialy expel the sub-optimal ones. This typically means expelling symbions in Clade C. This has been shown in (explain studies….)
Prevailing viewpoint is that very rare symbionts are unstable and don’t contribute much to coral colony fitness….. thus if corals are to survive heat stress it is generally believed that they either need to start with heat-tolerant D’s being dominant (?, or at least quite common) or would need to acquire them from the surrounding environment. -Please confirm that we have the data from your water samples to show that those D’s were not just floating around in the water column, but rather the only place they existed was in very very low #s within the colonies themselves?
What is known / expected about local protection’s influence on symbiont community? influence on survival through heat stress?
Danielle’s Notes:
Coral symbiosis is the foundation of coral reef ecosystems [16; Muller-Parker2015-sd].
The coral holobiont responds to environmental conditions, and is the unit that interacts with the broader reef community17
There is much genetic, functional, and response diversity within Symbiodinium
Although Symbiodinium is a single genus, it contains diversity similar to diversity found within other dinoflagellate orders6, and is divided into nine clades and hundreds of types18–20. There is much debate about species classifications within Symbiodinium, which has hampered species naming within Symbiodinium [21; but see 22) although Symbiodinium types are generally considered putative species [23. Symbiodinium types have distinct geographic distributions, host associations, and environmental optima24. Furthermore, total and relative abundance of Symbiodinium can vary among coral colonies, across environmental gradients, and over time25, with increased Symbiodinium abundance leading to increased environmental sensitivity and bleaching risk26. There are functional differences between Symbiodinium clades27, and Symbiodinium associations can range from mutualistic to neutral to parasitic based on Symbiodinium type as well as environmental conditions [11. Next-generation sequencing has revealed cryptic genetic diversity within symbiotic Symbiodinium28–30, and has allowed for long-term genetic and ecological comparisons of symbiont community structure31.Corals exhibit varying levels of symbiotic flexibility, but this flexibility comes with functional tradeoffs.
Corals that host flexible symbioses (generalists) may be more sensitive to environmental perturbations than those with intimate symbioses (specialists)32. Changes in photosynthetic efficiency during bleaching as well as bleaching resistance have been shown to correspond to distinct Symbiodinium phylotypes33. Clade D Symbiodinium are proported to have an enhanced thermal tolerance (Stat and Gates 2011), and repopulation of a coral host with clade D symbionts after a bleaching event is proposed to be a survival mechanism34–36. A history of thermal stress increased the prevalence of clade D Symbiodinium in a generalist coral species, but did not instigate similar changes in two specialist coral species37. Although the prevalence of clade D Symbiodinium increases during thermal stress and may increase thermal tolerance34, corals that house clade D symbionts may have slower growth rates8 or lower energy storage38. Furthermore, in an analysis conducted below the clade level, functional differences were found among types within clade C39.The adaptive bleaching hypothesis provides a testable hypothesis for bleaching causes and consequences, but hasn’t found extensive support
The adaptive bleaching hypothesis suggests that corals bleach in order to expel environmentally sub-optimal symbionts, followed by switching (picking up new symbionts from the environment) or shuffling (an internal change in dominant symbiont type or overall symbiont community structure) (Buddemeier and Fautin 1993, Baker 2001, Baker 2003, Buddemeier et al 2004). There is ample evidence for Symbiodinium shuffling (Baker et al 2004, Rowan 2004), and a recent study showed evidence for Symbiodinium switching (Boulotte et al 2016).The current paradigm of coral bleaching and recovery states that the stress must cease for coral to regain their symbiosis
Coral bleaching is the loss of obligate symbionts (Symbiodinium) from the coral tissue (Gates et al 1992, Douglas 2003). Thermal stress is the primary cause for coral bleaching, and can cause not only the breakdown of coral symbioses, but also cause coral mortality (Hoegh-Guldberg 1999, Abrego et al 2012, Stat et al 2013, Baker 2013). Thermal stress can be exacerbated by other environmental stressors (Cooper et al 2011, Béraud et al 2013, Maina et al 2008), and in turn, exacerbates ocean acidification (Gibbin et al 2015). The current paradigm of coral bleaching and resilience is that as environmental stress (such as warming) increases, corals begin to bleach. Extreme or long-lasting warming causes a complete breakdown of the coral symbioses, leading to expulsion of all (or nearly all) Symbiodinium from the coral host tissue. It has been shown that during bleaching, there is a window for recovery, that is, a certain amount of time during which the warming must cease and conditions must return to normal so that the coral can regain its symbionts. If the window for recovery passes without amelioration of the environmental conditions, the coral will starve and die. (Cunning et al 2016, Putnam et al 2017).The “transient microbiome” assembled by environmental anomalies can undergo rapid changes (Putnam et al 2017), providing symbiotic stochasticity which may build or weaken a coral’s capacity for resilience.
The “transient microbiome” assembled by environmental anomalies can undergo rapid changes (Putnam et al 2017), providing symbiotic stochasticity which may strengthen or weaken a coral’s capacity for resilience. While corals have been shown to change symbiotic partners during a bleaching event (Chen et al 2005, Jones et al 2008), there is often a quick return to pre-bleaching Symbiodinium communities after recovery (Thornhill 2005, LaJeunesse et al 2010), and persistence of stress-related changes to Symbiodinium community structure may require sustained environmental pressure (Baird et al 2007). Corals commonly host background Symbiodinium types in low levels (Correa et al 2009), but sub-dominant Symbiodinium communities are often unstable (Coffroth et al 2010). The importance of rare Symbiodinium types is currently under debate, and these rare types may be commensal (pass through coral’s holobiont with no harm or gain for either partner), parasitic (“cheaters”, or symbionts that take more than they give), or mutualistic (symbionts which support host function) (Parkinson et al 2015). Some research suggests that low-abundance Symbiodinium types have minimal functional significance to corals (Lee et al 2016), while other evidence supports the idea that the rare Symbiodinium biosphere is important for corals’ response to climate change (Boulotte et al 2016). However, shifts in Symbiodinium community diversity may still have a larger influence on coral resilience than the evolution of symbiont thermal tolerance (Baskett et al 2010). In other systems, other rare microbial species have been demonstrated to be disproportionally important to maintaining functional processes during environmental change (Shade et al 2014).Global coral bleaching is increasing, and the 2014-2017 event caused a catastrophic loss of corals around the globe.
There was up to 95% mortality in some regions during the 1997/1998 El Niño event (Glynn 1993). The 2014-2017 global coral bleaching event caused coral bleaching across the world’s oceans (Eakin 2016, Normile 2016), with up to 75% bleaching on some reefs in Hawaii, and at least some level of bleaching across 93% of the Great Barrier Reef (Minton et al 2015, GBRMPA 2016). Despite these staggering losses, some corals have the capacity to be resilient to these increasingly frequent mass-bleaching events (Hughes et al 2017).There is evidence for local adaptation in corals (Howells et al 2012, Logan et al 2013, Dixon et al 2015). Furthermore, in Orbicella annularis (a major Caribbean reef-builder), Symbiodinium biogeography correlates better with environmental patterns (i.e. chronic maximum summer temperature) than with coral host genetics (Kennedy et al 2016).
Eighty percent of coral species have horizontal symbiont uptake (Symbiodinium associations are formed anew with each coral generation from an environmental pool of symbionts)(CITE Nitschke Cites this statistic in abstract, but i’m having a hard time finding it. Other major paper on this topic is Baird et al 2009 ). Despite this, there is evidence for coevolution between coral and Symbidoinium (Thornhill et al 2014), although a Caribbean study showed that the structuring of host and symbiont populations were not congruent (Baums et al 2014).
Particulate and dissolved nutrients do not reduce coral health at a colony scale (Rocker et al 2017) - (this result just seems crazy to me… also they considered the fact that corals at moderate WQ sites - which was their worst WQ - had fast growth, less-dense skeletons, high symbiont densities and high lipid content. This seems like a mixed bag to me. High symbiont densities make a coral more sensitive to bleaching (Cunning). I’m not sure if skeletal density is good or bad, except it’s probably bad to have less dense skeletons during storms. They also found that dominant symbiont types differed among sites in one region (Burdekin) but thot the other (Whitsunday). Again, results & implications are a little unclear here as this isn’t the major focus of their paper.)
FYI - probably don’t include these points: 12. Thick-tissue corals may be less susceptible to coral bleaching and mortality due to their tissue biomass and associated energy reserves.
Thick-tissue corals (such as Platygyra) may be less susceptible to coral bleaching and mortality due to their tissue biomass and associated energy reserves (Loya et al 2001). Furthermore, self-shading can protect “understory” Symbiodinium, those which reside deeper in the coral’s tissue and consequently experiences less light stress, which can provide a symbiont reserve for repopulation and recovery (Kemp et al 2014).
- Coral host gene regulation can influence Symbiodinium stress levels Parkinson et al 2015 In a bleaching study with genetically different coral colonies and genetically similar Symbiodinium, symbionts that partnered with ‘adaptive hosts’, or those which altered the regulation of more genes during bleaching, were less stressed (Parkinson et al 2015). Indeed, coral transcription is correlated with the presence of different Symbiodinium genotypes (DeSalvo et al 2010), but it is unclear whether it is the host transcription or the Symbiodinium community that is the driver in this correlation.
Main text draft The symbiosis between coral and their single-celled dinoflagellate symbionts, Symbiodinium, is the foundation of reef ecosystems, and a critical element of reef resilience (16). Corals host a diverse community of Symbiodinium, ranging along a continuum from ‘selfish opportunistic symbionts’ (e.g. some clade D Symbiodinium) which are better suited to sustained environmental stress, to ‘intimately evolved symbionts’ which provide exceptional amounts of nutrition to their coral host (??? , ???). Diversity with the genus Symbiodinium is high, comparable to genetic variability among orders in other dinoflagellate taxa (6), and is divided hierarchically into clades, subclades, and types. Symbiotic flexibility and stability can be variable both within and among coral species (32, CITE?), and this can be a driver in determining “winers and losers” (40) during coral bleaching events. Coral bleaching is the breakdown of symbiosis, where Symbiodinium are expelled en masse from the tissues of their coral host. A coral’s susceptibility and resilience to bleaching is, in part, determined by fine-scale variability in their compliment of associated symbionts (39). Corals have been observed to recover from bleaching only if the underlying stress, such as ocean warming, abates.
Ocean warming events can cause massive losses of coral cover (CITE,CITE). The 2015-2016 El Niño, superimposed on nearly-ubiquitous tropical ocean warming, instigated the third global coral bleaching event (???). Our study location, Kiritimati Atoll (Christmas Island, Kiribati, Central Equatorial Pacific, Coordinates: 2, -157.4), was at the epicenter of this extreme El Niño event. Thermal anomalies were severe on Kiritimati, rapidly exceeding NOAA Coral Reef Watch’s Coral Bleaching Alert Level 1 (4 Degree Heating Weeks, DHW, a metric of cumulative thermal stress) and Alert Level 2 (8 DHW) thresholds, reaching an unprecedented (41) 25.7 DHW over a year-long bleaching event, demolishing most of the reef (???). Despite the massive mortality resulting from this extreme heat stress event, some corals survived.
Here, we assess coral symbiosis and survival during the massive 2015/2016 El Niño event. We tagged, sampled, and photographed the same coral colonies before, during, and immediately after the El Niño event. We assessed bleaching condition and survival for each coral colony, and used Illumina MiSeq ITS2 amplicon sequencing and 97% de novo OTU clustering to evaluate changes in Symbiodinium community structure. To investigate mechanisms underlying the ability of these corals to not only survive a year of continuous heat stress, but to recover in the interim, we assessed the relationship between human disturbance, pre-bleaching Symbiodinium community structure, and coral survival, as well as the timing of Symbiodinium community shifts throughout this El Niño event. We document, for the first time, corals that were able to visually recover from bleaching, and to regain their Symbiodinium communities during the course of an extreme heat stress event. These corals (family Faviidae; Platygyra sp. and Favites sp.) were bleached within two months of the onset of warming, but had visibly recovered after 10 consecutive months of intense warming. Previously, corals have been shown to recover from bleaching only after the external stress (e.g. warming) has subsided (CITE), implying that longer and more frequent stressors spell disaster for reefs worldwide. This unprecedented resilience mechanism…
